Exotic Plant Disease Threats to the New Zealand Avocado Industry and Climatic Suitability: a Review

Pathogens 1 25 was funded through a grant from The Ministry of spray drift. NZ Kiwifruit, Feb: 18-19. for Business and Innovation under the project Holland P, Maber J, May W, Malcolm C 1997. Exotic plant disease threats to the New Zealand avocado “Protecting NZ’s Environment from Pesticide Drift from orchard spraying. Proceedings industry and climatic suitability: a review Exposure”. of the New Zealand Plant Protection Conference. Pp. 112-118. Kerry R. Everett1,* and Brad Siebert2 REFERENCES Johnson D 1995. Drift from orchard airblast Bonds JAS, Leggett M 2015. A literature review applications: Integration and summary of 1 e New Zealand Institute for Plant & Food Research Limited, Private Bag 92169, Mt Albert, of downwind drift from airblast sprayers: 1993 and 1994 field studies. Spray Drift Task Auckland 1142, New Zealand development of standard methodologies and Force (SDTF) Report No. I95-004. Stewart 2New Zealand Avocado, PO Box 13267, Tauranga 3141, New Zealand a drift database. Transactions of the ASABE Agricultural Research Services, Inc. Macon, *Corresponding author: [email protected] 58: 1471-1477. MO, USA. Connell R, Woodward S, Zabkiewicz J, Moller H, Wearing A, Perley C, Rosin C, Abstract The avocado industry was established in New Zealand from several importations Hewitt A 2010. Shelterbelt interception Blackwell G, Campbell H, Hunt L 2007. dating back to 1907. Several serious pathogens found elsewhere in the world were not of agrichemicals: model and field results. Biodiversity on kiwifruit orchards: the imported. A literature review and internet search were conducted to determine what Aspects of Applied Biology 99: 443-448. importance of shelterbelts. Proceedings of the serious avocado pathogens are not present in New Zealand and the potential impact they Fritz BK, Hoffmann WC 2008. Collection 6th International Symposium on Kiwifruit, could have if they established. Relevant information was summarised for six pathogens efficiencies of various airborne spray flux Rotorua. determined to be the most serious of avocado and not known to be present in New Zealand: samplers used in aerial application research. Nufarm n.d. Driftstop. http://www.nufarm.com/ avocado sunblotch viroid (ASBVd); Pseudocercospora purpurea (cercospora spot); Raaelea Journal of ASTM international 5: 1-11. assets/37041/1/DriftStopBrochure.pdf lauricola (laurel wilt); Fusarium sp. (fusarium dieback); Phellinus noxius (brown root rot); Gaskin R, Manktelow D, Steele K 2006. Adjuvant Peterson J, Wolf T, Mazurek K, Caldwell B and Sphaceloma perseae (avocado scab). Laurel wilt, brown root rot, cercospora spot and and application technologies to minimise 2008. The movement of spray drift near a fusarium dieback could become established in New Zealand if the climate here becomes off-target drift from kiwifruit sprays. New live shelterbelt. Soils & Crops Conference, warmer but establishment of ASBVd and avocado scab (which are not restricted to hot Zealand Plant Protection 59: 217. Saskatoon, Saskatchewan, Canada, February climates) is more likely. Gaskin R, Manktelow D, May W 2007. Adjuvants 28-29, 2008. and air inclusion nozzles reduce hydrogen Raupach MR, Leys JF, Woods N, Dorr G, Cleugh Keywords Sphaceloma perseae, Pseudocercospora purpurea, brown root rot, Euwallacea sp., cyanamide spray drift in kiwifruit orchards. HA 2000. Modelling the effects of riparian Raaelea lauricola, Xyleborus glabratus, redbay ambrosia beetle, Fusarium sp., Avocado Proceedings of the 8th International vegetation on spray drift and dust: The role sunblotch viroid. Symposium on Adjuvants for Agrochemicals of local protection. Technical Report 29/00. (ISAA2007). Columbus, OH, USA, 6-9 Aug. CSIRO, Canberra, Australia. http://www.clw. 2007. csiro.au/publications/technical2000/tr29-00. Gaskin R, Manktelow D, May W 2009. Field pdf INTRODUCTION Avocados in New Zealand are affected studies to optimise spray deposits on Schep L, Temple W, Beasley M 2007. The The avocado (Persea americana) is a sub- by a number of plant pathogens, of which shelterbelts and minimise off-target drift. evaluation of hydrogen cyanamide-related tropical Lauraceous tree that produces oil rich the most common are two root invaders Report to NZ Kiwifruit Growers, Inc. SFF inquiries to the New Zealand National fruit. Avocados originate from middle America (Phytophthora cinnamomi and Verticillium Project # 06/090. July 2009. http://maxa.maf. Poisons Centre between 1990 and 2006. (Mexico, West Indies and Guatemala) and dahliae) and pathogens that cause rots in ripe govt.nz/sff/about-projects/search/06-090/ Clinical Toxicology 45: 360. avocado plants were first imported into Tauranga, fruit (Colletotrichum acutatum, Colletotrichum shelter-drift-report.pdf Schep L, Temple W, Beasley M 2009. The adverse New Zealand as seedlings in 1907 (Green gloeosporioides, Botryosphaeria dothidea, Gaskin R, Manktelow D, May B, Max S 2008. effects of hydrogen cyanamide on human 1927). Several more plants were imported to Neofusicoccum parvum (syn. B. parva) and Development of Best Practice to minimise health: an evaluation of inquiries to the New Tauranga and Wanganui in 1917, followed by the Phomopsis sp.). These pathogens have a wide host off-target drift from hydrogen cyanamide Zealand National Poisons Centre. Clinical importation of grafted avocados from California range and may have originated from infected sprays in kiwifruit orchards. New Zealand Toxicology 47: 58-60. to Gisborne and Tauranga in 1940 (White 2001). host material already present in New Zealand or Plant Protection 61: 153-158. Zhu H, Reichard DL, Fox RD, Brazee RD, Ozkan More recent importations of new rootstocks from infected avocado plant material imported in Gaskin R, Manktelow D, Cook S, May W, van HE 1996. Collection efficiency of spray and fruiting varieties from South Africa and 1907, 1917 and 1940. Most fungi that infect fruit Leeuwen R 2013. Effects of canopy density on droplets on vertical targets. Transactions of California took place since 1999. The ‘Hass’ to cause rots will also asymptomatically infect spray deposition in kiwifruit. New Zealand the ASABE 39: 415-422. variety is the most commonly grown avocado in vegetative tissue (Everett et al. 1999; Hartill & Plant Protection 66: 194-198. New Zealand and was probably imported with the Everett 2002; Everett et al. 2003). The first record Holland P, Maber J 1992. Reducing the problem batch of grafted avocados in 1940 (White 2001). of an avocado fruit rot was of C. gloeosporioides

©2018 New Zealand Plant Protection Society (Inc.) www.nzpps.org Refer to http://www.nzpps.org/terms_of_use.html New Zealand Plant Protection 71: 25-38 (2018) https://doi.org/10.30843/nzpp.2018.71.140 Pathogens 1 26

(Brien 1939), and the first record of a root disease The aim of this study was to collate relevant The main problems associated with this al. 1984). Seed transmission from ‘recovered’ was of Phytophthora cinnamomi (Zentmeyer information on serious avocado pathogens not disease are disease management costs, such as or symptomless trees can be as high as 95% 1965), then the vascular wilt pathogen V. dahliae currently present in New Zealand and their those required to ensure nursery material is (Wallace & Drake 1962). Spread by seed from (Fletcher 1976). The remaining commonly potential impact to the New Zealand avocado not infected, destroying infected trees in the fruit developing from flowers pollinated with occurring fruit rot pathogens were first reported industry if they were to establish in avocado- orchard showing symptoms, tests for detection of infected pollen (5%) was higher than from the by Boesewinkel (1982) (C. acutatum), Hartill growing regions of the country. asymptomatic infected trees, and yield reduction. pollen itself (1-4%) (Wallace & Drake 1962). (1987) (N. parvum, Phomopsis sp.) and Hartill et Presence of ASBVd can also restrict access to Foliar symptoms are more pronounced al. (1991a,b) (B. dothidea). METHODS some markets, such as the restriction of imports with increased temperature (da Graca & van Biosecurity measures for importation of An electronic literature search of Web of Science, from eight countries with records of ASBVd by Vuuren 1981b) suggesting an adaptation to hot nursery stock into New Zealand date back to CABI and Google databases was conducted on 2 Costa Rico in 2015 (Anonymous, 2015). ASBVd climates. Although New Zealand has a relatively 1889, when fumigation vaults were constructed, February 2018 using the terms avocado or Persea causes skin distortions and chlorotic patches cool climate, the viroid is expected to survive according to Helson (1966). Since as early as AND fung* or plant and pathogen*. Resultant rendering the disfigured avocados unmarketable. wherever avocado trees grow (Perez et al. 2017). 1966, imported plants were inspected at the publications were obtained and the literature ASBVd affects leaves and shoots similarly, causing Therefore, the disease could establish where New Zealand border and fumigated with methyl listed in those papers was used to access literature distortions and chlorotic patches. ASBVd can also avocados are grown in New Zealand, in the bromide if any pests were detected (Helson beyond the scope of the electronic searches. infect asymptomatically, depending on the host Northland, Whangarei, Bay of Plenty, Hawke’s 1966). Post inspection and treatment the plants References in the first author’s collection were cultivar, environmental conditions and viroid Bay and Nelson districts. were placed in post-entry quarantine for 12 also accessed. The Manaaki Whenua Landcare strain (Saucedo-Carabez et al. 2014). Infected months and all plants showing disease symptoms database (www.landcareresearch.co.nz) was trunk bark can have a scaly appearance referred Avocado scab (Sphaceloma perseae) during this period were destroyed. Since 1993, accessed to determine what pathogens were not to as ‘crocodile’ bark. A study by da Graca et al. in Sphaceloma perseae is listed in the Crop Protection importations of avocado plant material have present in New Zealand. Only those avocado 1983 found the effect of ASBVd-infection on the Compendium (CABI 2014a) as present in been subject to additional biosecurity measures pathogens not previously reported in New overall crop was severe resulting in over half the the Philippines, Taiwan, Guinea, Morocco, imposed by the Ministry for Primary Industries Zealand that are considered to have the potential harvested fruit downgraded due to poor quality South Africa, Zambia, Zimbabwe, Bermuda, Standard 155.02.06 Importation of Nursery Stock to become a serious problem if they establish are (although the overall reduction in yield was only Mexico, USA (Florida, Texas), Barbados, Costa issued as an import health standard pursuant to included. These decisions were made according 30%). Desjardins et al. (1987) found the yield of Rica, Cuba, Dominica, Dominican Republic, section 24A of the Biosecurity Act 1993 (MPI to an examination of the publications and the fruit from ASBVd-infected trees may be reduced El Salvador, Guadeloupe, Guatemala, Haiti, 2014). These measures along with improved authors’ expert opinion. by as much as 95%. More recently, Saucedo- Honduras, Jamaica, Nicaragua, Panama, Puerto diagnostic techniques are likely the reason there Carabez et al. (2014) reported the yield of ‘Hass’ Rico, Argentina, Brazil (Espirito Santo, Rio have been no new records of avocado diseases RESULTS was reduced by 75% in symptomatic trees and Grande do Sul), Guyana, Peru and Venezuela. since 1991. Over 70 papers were selected as a result of the 30% in symptomless trees. Trees can be stunted Avocado scab causes superficial cosmetic Diseases of avocado not found to date in above search. Information on current disease and growing points can die back. ASBVd can also damage to fruit, reducing its marketability. New Zealand are: avocado sunblotch viroid range, hosts, infection pathways and possible cause premature leaf and flower fall. The main Crop losses of up to 53% have been reported (ASBVd); avocado scab (Sphaceloma perseae); impact if established in New Zealand is presented pathways of transmission of ASBVd are through (Vidales 1996). Lesions may also affect leaves, cercospora spot (Pseudocercospora purpurea); for each organism. the use of graft material during propagation but reduction in yield from leaf infection has laurel wilt (Raaelea lauricola); fusarium dieback and infected seed used for rootstocks. However, not been reported. The most important impact (Fusarium sp.); and Phellinus noxius. Avocado sunblotch viroid (ASBVd) natural disease transmission can occur by root if it established in New Zealand would be a An early record of S. perseae (avocado ASBVd is reported to be present in Israel, Ghana, grafting. Mechanical transmission is rare although restriction of market access for New Zealand scab) in New Zealand (Hartill 1991a), was South Africa, Spain, Mexico, the United States of ASBVd can be spread on sap-contaminated tools avocados to countries or regions that do not have disproved by Everett et al. (2011), following America (USA; California, Florida), Peru, Costa (e.g. injection equipment, pruning saws and this disease such as Australia, Europe and USA re-examination and pathogenicity tests of the Rica, Guatemala, Venezuela and Australia (CABI clippers). Desjardins et al. (1979) reported a low (California) (Everett et al. 2011). specimens deposited in the Manaaki Whenua 2014b; EPPO 2016). rate of spread caused by infected pollen carried Scab symptoms can be similar to physical Landcare Research Herbarium and International ASBVd is known to naturally infect only by bees (1–4%). In that study, the pollen caused damage caused by other means, such as wind Collection of Microorganisms from Plants one host, Persea americana (avocado). Under infection of developing fruit without the trees rub. Characteristic symptoms of scab are circular (ICMP). A record of ASBVd detected in 1999 by experimental conditions, however, ASBVd was being affected (Desjardins et al. 1987). Trees lesions on the surface of the fruit that can converge the Ministry of Agriculture and Forestry (MAF) transmitted to plants of other members of the were indexed for sunblotch infection by grafting into larger areas of rough corky tissue, circular was also disproven following a joint avocado Lauraceae family using a bark-patch grafting with a viroid free scion. Infected seed used for lesions on the peduncles, and ‘scabby’, hard, industry and MAF biosecurity survey conducted technique (da Graca & van Vuuren 1980; da rootstocks taken from symptomless trees, can protruding, circular lesions on the underside of during 2009 (Pugh & Thomson 2009). Graca & van Vuuren 1981a). result in outbreaks of sunblotch (Desjardins et the leaves. Leaf symptoms are difficult to find Pathogens 1 28 through basic field monitoring as infections petioles may also be infected during spring and and coalesce to form large brown patches. On are mostly in the top of the canopy (Palmateer early summer (Palmateer 2006). Temperatures immature fruit, the first symptoms are small (c. 3 2006). A DNA test for avocado scab is available in avocado-growing districts of New Zealand are mm) greenish-white, superficial blemishes. Once for nursery plants and fruit (Everett et al. 2011). usually within the range suitable for infection fruit are mature, the disease is characterised by Movement of infected nursery plants probably during fruit set and early growth (HortPlus slightly sunken brown blotches (c. <6 mm) that presents the highest risk of spreading avocado 2018). The conidia of the closely related citrus may coalesce and form small surface cracks scab. Plant material for propagation can only be scab fungus, Elsinoë fawcettii, required 1.5–2.5 (Pegg et al. 2002). imported into New Zealand as dormant cuttings hours in free water to germinate and infect citrus Spores are released and spread by rainfall from or tissue cultures. Imported material must also be (Whiteside 1975). Infection can occur during infected fruit, leaves and stems. Fruit are most grown in a post-entry quarantine facility for 12 periods of rain or heavy morning dew, both of susceptible to infection in early summer, and months and inspected regularly for symptoms. which are frequent during the period of fruit spores are more difficult to isolate from lesions as This level of inspection would be expected to susceptibility in New Zealand (HortPlus 2018). they age. Spores may be spread on contaminated detect new infections and any existing lesions on Humidity had no effect on disease progress even equipment and by leaf material (Dann et al. Figure 1 Average monthly temperatures for the trunk or twigs thus minimising the risk of when it was as low as 30% (Marroquin-Pimentel 2013). Tzaneen, South Africa and Northland, New importation of avocado scab by this pathway. The 1998), and is unlikely to be a limiting factor for A relationship between spore release, Zealand. Data from http://www.meoweather. Import Health Standard (IHS) for fresh fruit into infection in New Zealand. temperature and humidity was described by com/h (South Africa) and from MetWatch New Zealand allows imports only from Australia Darvas (1982). Spore release was highest at 18°C Online (HortPlus 2018) (New Zealand). and Tonga (MAF 2014), which are not known Cercospora spot (Pseudocercospora purpurea) and declined gradually as temperatures increased to have avocado scab so the risk of importing Pseudocercospora purpurea is listed in the Crop to 25°C (the lowest and highest temperatures avocado scab on fruit through this commercial Protection Compendium (CABI 2014d) as being measured respectively). Spore release was Laurel wilt (Ra aelea lauricola) pathway is low. Infected mature fruit probably present in India (Sikkim), Japan, Philippines, positively correlated with humidity up to 84%. The fungus Raaelea lauricola is listed in the represent a low risk as most sporulation occurs Cameroon, Congo Democratic Republic, Côte Temperatures during early spring are generally CABI Crop Protection Compendium (CABI up to 2–3 months after fruit set (Palmateer 2006). d’Ivoire, Guinea, Kenya, South Africa, Bermuda, lower than 18°C in the avocado-growing 2014c) as present in some eastern states of the Avocado seeds are not likely to be contaminated Mexico, USA (Florida, Georgia, Mississippi) districts of New Zealand (HortPlus 2018). In the USA (Alabama, Florida, Georgia, Mississippi, with avocado scab, because, as far as is known, it Dominica, El Salvador, Honduras, Jamaica, Tzaneen region of South Africa, most infections South Carolina). is not seed transmitted. Nicaragua, Panama, Puerto Rico, Trinidad and occurred between November and January but the Hosts are members of the Lauraceae family, Avocado scab produces spores on fruit, leaves Tobago, United States Virgin Islands Argentina, temperature minima and maxima for infection including Persea americana (Mayfield et al. 2008), and twigs during the early stages of infection. Bolivia, Brazil, (Sao Paulo), Chile, Guyana, Peru, were not determined (Darvas 1982). After March, Cinnamomum camphora (camphor laurel), Litsea Spores are spread by rain and wind but also Venezuela and Palau. There are also records of no new infections were recorded (Darvas 1982), sp., Persea borbonia (bay laurel), Persea humilis on contaminated equipment (e.g. pruning cercospora spot in Australia (Peterson & Grice presumably because the temperatures were too (silk bay), Sassafras albidum (common sassafras) saws, clippers, leaves caught on hydra-ladders, 1992), Costa Rica, Cuba, Dominican Republic, low for infection to occur. Precipitation occurs (CABI 2014c). picking bags and fruit bins) and by leaf material Guadeloupe, Guatemala and USA (Hawaii, throughout the year with the highest rainfall in Laurel wilt affects avocados causing wilting contaminating workers’ clothing. south-eastern states) (Crous & Braun 2003). January (182 mm average) and the lowest in July of terminal leaves that then turn brown. Wilting Avocado is the only known host of avocado Fruit losses due to cosmetic damage can be (10 mm average) (https://en.climate-data.org/ can be branch specific, with some branches scab (Jenkins 1934) so establishment in New up to 69% in unsprayed orchards in South Africa location/15345/); thus, rainfall is unlikely to limit unaffected. Avocado leaves defoliate 2–3 months Zealand would be limited to avocado trees (Darvas & Kotze 1987). All commercial cultivars infection. Monthly average temperatures in New after the onset of symptoms. Affected avocado in orchards, public places and home gardens. of P. americana are affected (Chupp 1954; Crous Zealand (Fig. 1) suggest that the temperatures sapwood is stained reddish brown to bluish grey Infection occurs at temperatures between 10 & Braun 2003). In Tzaneen, South Africa, may be too low for the establishment of this (Ploetz et al. 2012). Eventually, the entire tree and 26°C (Marroquin-Pimentel 1999; Vidales commercial losses from sprayed orchards over a disease. dies over a period of weeks to several months et al. 1999; Marroquin-Pimentel 2000). Fruit 6-year period ranged from 0 to 12% for ‘Fuerte’, (Evans et al. 2010). These same authors estimated are susceptible to infection immediately after set ‘Edranol’, ‘Hass’ and ‘Ryan’ cultivars (Darvas economic losses from laurel wilt in Florida based until reaching a size of 20–29 (W) x 24–39 (H) 1982). on a $US30M per annum industry, reductions mm (Avila-Quezada et al. 2003), or until half Characteristic symptoms on leaves are angular in property values and increased management size (about 30 (W) x 50 (H) mm) (Pernezny & leaf spots, initially 1–2 mm diameter surrounded costs. If laurel wilt were to affect 50% of trees in Marlatt 2007). Young leaves are also susceptible by a small yellow halo that first appears on the Florida, the estimated cost would be $US182M, to infection, but become resistant after a month lower side of mature to older leaves. Spots and $US271M if 75% of trees were affected. (Pernezny & Marlatt 2007). Twigs, peduncles and eventually appear on the top surface of leaves Pathogens 1 29 through basic field monitoring as infections petioles may also be infected during spring and and coalesce to form large brown patches. On are mostly in the top of the canopy (Palmateer early summer (Palmateer 2006). Temperatures immature fruit, the first symptoms are small (c. 3 2006). A DNA test for avocado scab is available in avocado-growing districts of New Zealand are mm) greenish-white, superficial blemishes. Once for nursery plants and fruit (Everett et al. 2011). usually within the range suitable for infection fruit are mature, the disease is characterised by Movement of infected nursery plants probably during fruit set and early growth (HortPlus slightly sunken brown blotches (c. <6 mm) that presents the highest risk of spreading avocado 2018). The conidia of the closely related citrus may coalesce and form small surface cracks scab. Plant material for propagation can only be scab fungus, Elsinoë fawcettii, required 1.5–2.5 (Pegg et al. 2002). imported into New Zealand as dormant cuttings hours in free water to germinate and infect citrus Spores are released and spread by rainfall from or tissue cultures. Imported material must also be (Whiteside 1975). Infection can occur during infected fruit, leaves and stems. Fruit are most grown in a post-entry quarantine facility for 12 periods of rain or heavy morning dew, both of susceptible to infection in early summer, and months and inspected regularly for symptoms. which are frequent during the period of fruit spores are more difficult to isolate from lesions as This level of inspection would be expected to susceptibility in New Zealand (HortPlus 2018). they age. Spores may be spread on contaminated detect new infections and any existing lesions on Humidity had no effect on disease progress even equipment and by leaf material (Dann et al. Figure 1 Average monthly temperatures for the trunk or twigs thus minimising the risk of when it was as low as 30% (Marroquin-Pimentel 2013). Tzaneen, South Africa and Northland, New importation of avocado scab by this pathway. The 1998), and is unlikely to be a limiting factor for A relationship between spore release, Zealand. Data from http://www.meoweather. Import Health Standard (IHS) for fresh fruit into infection in New Zealand. temperature and humidity was described by com/h (South Africa) and from MetWatch New Zealand allows imports only from Australia Darvas (1982). Spore release was highest at 18°C Online (HortPlus 2018) (New Zealand). and Tonga (MAF 2014), which are not known Cercospora spot (Pseudocercospora purpurea) and declined gradually as temperatures increased to have avocado scab so the risk of importing Pseudocercospora purpurea is listed in the Crop to 25°C (the lowest and highest temperatures avocado scab on fruit through this commercial Protection Compendium (CABI 2014d) as being measured respectively). Spore release was Laurel wilt (Ra aelea lauricola) pathway is low. Infected mature fruit probably present in India (Sikkim), Japan, Philippines, positively correlated with humidity up to 84%. The fungus Raaelea lauricola is listed in the represent a low risk as most sporulation occurs Cameroon, Congo Democratic Republic, Côte Temperatures during early spring are generally CABI Crop Protection Compendium (CABI up to 2–3 months after fruit set (Palmateer 2006). d’Ivoire, Guinea, Kenya, South Africa, Bermuda, lower than 18°C in the avocado-growing 2014c) as present in some eastern states of the Avocado seeds are not likely to be contaminated Mexico, USA (Florida, Georgia, Mississippi) districts of New Zealand (HortPlus 2018). In the USA (Alabama, Florida, Georgia, Mississippi, with avocado scab, because, as far as is known, it Dominica, El Salvador, Honduras, Jamaica, Tzaneen region of South Africa, most infections South Carolina). is not seed transmitted. Nicaragua, Panama, Puerto Rico, Trinidad and occurred between November and January but the Hosts are members of the Lauraceae family, Avocado scab produces spores on fruit, leaves Tobago, United States Virgin Islands Argentina, temperature minima and maxima for infection including Persea americana (Mayfield et al. 2008), and twigs during the early stages of infection. Bolivia, Brazil, (Sao Paulo), Chile, Guyana, Peru, were not determined (Darvas 1982). After March, Cinnamomum camphora (camphor laurel), Litsea Spores are spread by rain and wind but also Venezuela and Palau. There are also records of no new infections were recorded (Darvas 1982), sp., Persea borbonia (bay laurel), Persea humilis on contaminated equipment (e.g. pruning cercospora spot in Australia (Peterson & Grice presumably because the temperatures were too (silk bay), Sassafras albidum (common sassafras) saws, clippers, leaves caught on hydra-ladders, 1992), Costa Rica, Cuba, Dominican Republic, low for infection to occur. Precipitation occurs (CABI 2014c). picking bags and fruit bins) and by leaf material Guadeloupe, Guatemala and USA (Hawaii, throughout the year with the highest rainfall in Laurel wilt affects avocados causing wilting contaminating workers’ clothing. south-eastern states) (Crous & Braun 2003). January (182 mm average) and the lowest in July of terminal leaves that then turn brown. Wilting Avocado is the only known host of avocado Fruit losses due to cosmetic damage can be (10 mm average) (https://en.climate-data.org/ can be branch specific, with some branches scab (Jenkins 1934) so establishment in New up to 69% in unsprayed orchards in South Africa location/15345/); thus, rainfall is unlikely to limit unaffected. Avocado leaves defoliate 2–3 months Zealand would be limited to avocado trees (Darvas & Kotze 1987). All commercial cultivars infection. Monthly average temperatures in New after the onset of symptoms. Affected avocado in orchards, public places and home gardens. of P. americana are affected (Chupp 1954; Crous Zealand (Fig. 1) suggest that the temperatures sapwood is stained reddish brown to bluish grey Infection occurs at temperatures between 10 & Braun 2003). In Tzaneen, South Africa, may be too low for the establishment of this (Ploetz et al. 2012). Eventually, the entire tree and 26°C (Marroquin-Pimentel 1999; Vidales commercial losses from sprayed orchards over a disease. dies over a period of weeks to several months et al. 1999; Marroquin-Pimentel 2000). Fruit 6-year period ranged from 0 to 12% for ‘Fuerte’, (Evans et al. 2010). These same authors estimated are susceptible to infection immediately after set ‘Edranol’, ‘Hass’ and ‘Ryan’ cultivars (Darvas economic losses from laurel wilt in Florida based until reaching a size of 20–29 (W) x 24–39 (H) 1982). on a $US30M per annum industry, reductions mm (Avila-Quezada et al. 2003), or until half Characteristic symptoms on leaves are angular in property values and increased management size (about 30 (W) x 50 (H) mm) (Pernezny & leaf spots, initially 1–2 mm diameter surrounded costs. If laurel wilt were to affect 50% of trees in Marlatt 2007). Young leaves are also susceptible by a small yellow halo that first appears on the Florida, the estimated cost would be $US182M, to infection, but become resistant after a month lower side of mature to older leaves. Spots and $US271M if 75% of trees were affected. (Pernezny & Marlatt 2007). Twigs, peduncles and eventually appear on the top surface of leaves Pathogens 1 30

These figures assume property value declines as of the living tree by the redbay ambrosia beetle, et al. 2012). Further examination has shown styraciua, Persea americana, Platanus racemosa, well as direct loss of income. the fungus produces conidia formed in fruiting that molecular phylogenetics distinguishes Camellia semiserrata); death of mature trees The vector, Xyleborus glabratus (redbay structures called sporodochia, upon which both six morphologically identical clades of F. was observed for three of these (Q. robur, A. ambrosia beetle), has historically been reported the beetle and its larvae feed. The beetle carries euwallaceae, of which at least four attack and negundo and R. communis) (Eskalen et al. 2013). to only invade dead trees of several plant fungal spores from tree-to-tree in specialised reproduce in avocado (O’Donnell et al. 2016). In A further eight reproductive hosts were found families (including Lauraceae, Dipterocarpaceae, pouches called mycangia. The fungi multiply addition to F. euwallaceae, found in Israel and the in Israel (Quercus ithaburensis, Q. calliprinos, Q. Fagaceae and Fabaceae) in its natural habit inside these mycangia in a yeast phase, nourished Los Angeles basin of Southern California, there pedunculiora, Morus alba, Platanus occidentalis, (Rabaglia et al. 2006). However, only since by secretions from surrounding gland cells are at least a further four unnamed Fusarium P. orientalis, Acer obutsifolium, A. pseudopltanus arriving in the south-eastern USA (SE USA), (Fraedrich et al. 2008; Harrington et al. 2011). species; Fusarium sp. AF-6 and AF-8 in Miami- (Mendel et al. 2017). has this beetle been reported to infest live No studies on the temperature range required Dade County, Florida; Fusarium sp. AF-7 in Avocado trunks attacked by PSHB exhibit trees. In 2003, large stands of bay laurel were for survival and reproduction of R. lauricola Queensland, Australia; and Fusarium sp. AF-12 ‘sugar volcanoes’ consisting of perseitol, a observed to wilt and die. Mortality was shown were found in the literature examined. The in San Diego and Orange Counties, California polyol, and possibly its 7-carbon sugar form to have resulted from infestation by X. glabratus, modelling of the spread of this fungus in the SE (O’Donnell et al. 2015). The Kuroshio shothole D-mannoheptulose (Minchin et al. 2015). followed by pathogenesis by the fungal pathogen USA used temperature parameters determined beetle (KSHB) has been shown to vector Fusarium Excretions 1–15 cm in diameter and 0.5–5 R. lauricola (Fraedrich et al. 2008). The insect for the vector, based on the described range in its sp. AF-12 (Dodge et al. 2017). These other cm high surround entry holes (Eskalen et al. vector was able to infest live plants of common native habitat (India, southern Japan, Myanmar associations cause less damage than F. euwallaceae 2013). Exit holes surrounded by small tubes sassafras, swamp bay (Persea palustris), camphor and Taiwan) (Koch & Smith 2008). According and PSHB (Kasson et al. 2013) although more of compacted sawdust can be seen after the laurel, silk bay, gulf licaria (Licaria trianda), to that model, the climate of coastal areas in the recent reports are that KSHB and Fusarium sp. emergence of adults (Mendel et al. 2012). pondberry (Lindera melissifolia) and pondspice SE USA was suitable for the establishment and AF-12 also cause a severe dieback disease in San Initial trunk infection is followed by wilting (Litsea aestivalis) which were then killed by the spread of the insect. The climate in both the Diego county and Northern Mexico (Dodge et of branches and discolouration of leaves, wilting fungus (Fraedrich et al. 2008; Smith et al. 2009; natural habitat and in the SE USA is warmer than al. 2017). KSHB has also been found in Santa and collapse of heavily bearing branches. PSHB Fraedrich et al. 2011; Hughes et al. 2011; Hughes in New Zealand; therefore, it is possible that the Barbara and San Luis Obispo Counties. Recently, constructs its galleries in xylem, thus growth et al. 2012; Bates et al. 2013; Ploetz & Konkol beetle would not be ideally suited to the New F. euwallaceae and PSHB have been reported for of the fungal symbiont can obstruct water 2013). Most members of the Lauraceae family Zealand climate, reducing chances of successful the first time attacking Platanus × acerifolia in transport causing wilting and dieback of the that have been tested are susceptible to laurel establishment and spread. the KwaZulu/Natal National Botanical Gardens host tree (Freeman et al. 2013). Large branches wilt (Pena et al. 2012). Camphor laurel is the only in South Africa (Paap et al. 2018). Two other are not as seriously aﬀected, thus only small one of these host species present in New Zealand Fusarium dieback fungi (Paracremonium pembeum and Graphium diameter branches exhibit severe symptoms. (Allan Herbarium 2000). However, there are Fusarium euwallaceae (Freeman et al. 2013) is euwallaceae) have been associated with fusarium Tree mortality has been reported (Freeman et several additional native and ornamental vectored by ambrosia beetles in the Euwallaceae dieback, and on inoculated shoots of avocado al. 2012), presumably of small trees. Fusarium members of the Lauraceae family that are likely fornicatus species complex (Na et al. 2018). These P. pembeum produced larger lesions than both euwallaceae survives in mycangia (small sacs) of hosts, including tawa and taraire (Beilschmiedia beetles are morphologically indistinguishable, F. euwallaceae and G. euwallaceae (Lynch et al. the PSHB (Freeman et al. 2012a), and, if similar tawa and B. tarairi). and can only be identified by sequencing the 2016). to other fungi vectored by ambrosia beetles, is The first detection of the vector in USA was mitochondrial cytochrome oxidase I (COI) Naturally spread F. euwallaceae has been nurtured there in a yeast form by secretions from in 2002. The spread of laurel wilt has exceeded locus by which they have been assigned the found causing symptoms on 112 tree species in gland cells of the insect (Fraedrich et al. 2008; that predicted in models (Koch & Smith 2008), names polyphagous shothole borer (Euwallacea 40 families in botanical gardens in California Harrington et al. 2011). The fungus also survives possibly because of human-assisted spread of sp. nr. fornicatus #1, PSHB) (Eskalen et al. 2013; (Eskalen et al. 2013), and in Israel 52 tree species in infected plants within galleries made by the infected logs as firewood throughout the SE O’Donnell et al. 2015) and Kuroshio shot hole from 26 botanical families (Mendel et al. 2017). PSHB. USA. In Florida, laurel wilt spread at the rate of borer (Euwallacea sp. nr. fornicatus #5, KSHB) Families with the highest number of infected In Israel, the major commercial avocado 32–48 km per year (Evans et al. 2010). Laurel wilt (O’Donnell et al. 2015; Stouthamer et al. 2017) species were the Aceraceae, Fabaceae and cultivars ‘Hass’, ‘Pinkerton’ and ‘Ettinger’ were took 10 years from the first detection in 2002 to in California. Euwallacea nr. fornicatus found in Fagaceae. attacked by the vector and the fungus, with ‘Hass’ invade commercial avocado orchards (Kendra et avocado trees in Israel (Mendel et al. 2017) was in Only 19 species were reproductive hosts for being the most susceptible. The fungus had been al. 2013). the same clade as PSHB (Stouthamer et al. 2017) PSHB (Acer buergerianum, A. macrophyllum, isolated from trees on 15 grower properties in the Both the insect vector and the fungus survive and is Euwallacea sp. nr. fornicatus #1. A. negundo, A. palmatum, A. paxii, Ilex coastal plain of central Israel by 2012 (Freeman in tunnels burrowed into wood of a suitable host. This fungus and its associated ambrosia beetle cornuta, Ricinus communis, Albizia julibrissin, et al. 2012b). The beetle–fungus complex has As the wood decays, the available nutrients for vectors have been described as causing a serious Castanospermum australe, Cercidium oridum, C. become a serious threat to the avocado industry the fungus decline, until eventually the pathogen dieback disease in Israel (Mendel et al. 2012; × sonorae, Erythrina corallodendron, Parkinsonia in that country (Freeman et al. 2012b; Mendel et is replaced by saprotrophs. During colonisation Mendel et al. 2017) and California (Eskalen aculeata, Quercus agrifolia, Q. robur, Liquidambar al. 2012). Pathogens 1 31

PSHB was first collected from several tree Acacia confusa, Araucaria cunninghamii (hoop and sub-tropical climates. In Taiwan, the disease detecting and reporting disease symptoms early. species in California in 2003 without an pine), Bauhinia variegata (mountain ebony), is not found at elevations >1000 m despite Laurel wilt and fusarium dieback are both associated disease. An associated Fusarium sp. Calophyllum inophyllum (Alexandrian laurel), the availability of susceptible host species, new, emerging diseases. Laurel wilt is the most disease was first observed in backyard avocado Camellia sinensis (tea), Casuarina equisetifolia presumably because it is too cold for the fungus aggressive and incursive plant pathogen of trees and woody ornamentals in 2012. By 2013, (casuarina), Coea sp. (coffee), Ficus microcarpa to grow, infect or survive (Ann et al. 1999; Ann avocados recorded worldwide. The current F. euwallaceae. was recovered from 54% (207 out (Indian laurel tree), Garcinia mangostana et al. 2002). distribution of the fungi causing laurel wilt and of 335) of trees found to be infested by PSHB (mangosteen), Podocarpus macrophyllus (long- fusarium dieback is in climates warmer than during an intensive survey of two botanical leaf podocarpus), Salix babylonica (weeping DISCUSSION New Zealand but there is still a risk that they gardens adjacent to the first sighting of PSHB willow), Tectona grandis (teak) and eobroma ASBVd infects avocados in a number of countries could establish here, especially if New Zealand (Eskalen et al. 2013). Fusarium euwallaceae is cacao (cocoa) (CABI 2014a). with climates similar to New Zealand so there is becomes warmer due to climate change. Usually primarily spread by the vector, which flies from Phellinus noxius causes considerable losses to a high risk of it establishing in New Zealand. Of ambrosia beetles attack declining or dead trees tree to tree, and by human-assisted movement of avocado growers in Taiwan every year (Ann et particular concern is its possible importation (Na et al. 2018). Both these diseases are vectored affected wood. al. 2002) while rows of dead avocado trees were in fruit from symptomless plants or seeds. New by ambrosia beetles that attack healthy trees. It Both Israel and California have warmer first noticed in Queensland, Australia in 2001 Zealand only imports fresh avocados from areas has been hypothesised that this is the effect of summers than New Zealand, but winter mean (Dann et al. 2009). Examination of the collar of free of ASBVd in Australia and from Tonga vectors being exposed to naïve and new hosts, daily temperatures are similar (Te Puke, c. 9°C, dead trees in Queensland revealed a ‘stocking’ of which does not have ASBVd, yet this pathway which produces confusing olfactory cues and Metwatch Online (HortPlus 2018); Ventura brown mycelium extending up the trunk, binding remains a risk as more fruit imports from other results in invasion of healthy tissue (Mendel et al. County California c. 12°C, http://www.usa.com/ together twigs, soil, and stones, sometimes with countries are likely to be considered in the future. 2017). Thus, the establishment of these vectors ventura-county-ca-weather.htm; Israel coastal a white margin. Eventually the ‘stocking’ turned Avocado seed for sowing can only be imported could have unexpected outcomes for the native plains 12°C, eastern valleys 13°C (Homsky 1995). black. The wood beneath the stocking was brown from the USA, which does report the presence vegetation of New Zealand such as new hosts Because winter temperatures are those that affect with white patches. A survey in Queensland of ASBVd. The measures specified in the IHS being attacked. the range of ambrosia beetles (Formby 2014), it (Australia) during 2007–2009 found P. noxius (MPI 2018) must be strictly adhered to ensure Brown root rot and cercospora spot are less will be necessary to determine if the c. 3°C lower in 17/18 properties on the Atherton Tableland, that ASBVd is not introduced. Illegal imports of likely than ASBVd or avocado scab to establish in mean monthly temperature is critical to the 3/5 in the Childers/Bundaberg area, and one seed for rootstocks or fruit from infected regions the relatively cool New Zealand climate. However, survival of Euwallacea spp. in order to estimate orchard at Maleny. Two orchards in northern are probably the pathways with the most risk the climate in Northland can experience likely establishment risk in New Zealand. New South Wales were also affected. Of the 23 of introducing ASBVd into New Zealand. The above-average temperatures as can various infected properties surveyed, about 10% of trees industry’s High Health Scheme also requires microclimates in other avocado production areas Phellinus noxius (Brown root rot) died on four severely affected orchards, with an avocado nurseries to undertake ASBVd testing in New Zealand so any potential for establishment Phellinus noxius is listed in the CABI Crop estimated economic loss of $AUD5400/ha. If left of the plants they propagate as an early-warning needs to be confirmed experimentally or with the Protection Compendium (2014a) as being present unmanaged, loss of an entire orchard is possible disease-screening programme. use of predictive models before firm conclusions in China, India (Assam, Karnataka, Kerala, (Dann et al. 2009). Environmental parameters suitable for can be made. Tamil Nadu, Tripura, Uttar Pradesh), Indonesia Phellinus noxius produces air-borne infection by avocado scab are found where (Java, Sumatra), Japan (Ryukyu Archipelago), basidiospores in bracket fungi type fruiting avocados are grown in New Zealand, and there is CONCLUSIONS Malaysia (Peninsular Malaysia, Sabah, Sarawak), structures, which can be dispersed widely. a high likelihood of establishment. There are few Avocado exports were worth $147.5 million to Myanmar, Pakistan, Philippines, Singapore, Sri Basidiospores infect wounded tissue such as commercial trade pathways for this pathogen, the New Zealand economy in the 2016 season, Lanka, Taiwan, Vietnam, Angola, Benin, Burkina pruning wounds and cut-off stumps. In Australia, yet the risk remains so industry vigilance and of which $125 million was earned from the Faso, Cameroon, Central African Republic, these fruiting structures have not been observed crop monitoring must continue. Industry Australian market (Aitkin & Warrington 2017). Congo Democratic Republic, Côte d’Ivoire, on avocados, but the epidemic may have been vigilance consists of formal crop monitoring If avocado scab were to establish in New Zealand, Gabon, Ghana, Kenya, Nigeria Sierra Leone, started by basidiospores from infected native by accredited pest monitors through the this lucrative market could be at risk, because Tanzania, Togo, Uganda, Costa Rica, Cuba, trees adjacent to the avocado orchards. Tree-to- AvoGreen® programme (Anonymous 2018) and S. perseae is not present in Australia. The main Puerto Rico, American Samoa, Australia (New tree spread is by root contact with adjacent trees is mandatory for all export registered orchards. impact of laurel wilt, fusarium dieback and South Wales, Queensland), Fiji, Micronesia, (Ann et al. 2002; Dann et al. 2009). Many of these trained pest scouts are also part Phellinus noxius would be on avocado yields Niue, Northern Mariana Islands, Papua New The fungus does not survive or spread at of the industry’s First Detector Network that because none of these diseases infect fruit. The Guinea, Samoa, Solomon Islands and Vanuatu. low temperatures. The optimal temperature for encourages early reporting of unusual pest and cost of yield losses, monitoring, removal and Phellinus noxius has a wide host range, mycelial growth is above 30°C and there was disease observations. The regular distribution destruction of infected trees if these diseases affecting 200 tree species belonging to 59 families, no growth at 8°C. This thermal range could of exotic pest and disease awareness material to establish in New Zealand is likely to be expensive. including Persea americana (Ann et al. 2002), explain the restriction of P. noxius to tropical growers also helps promote the importance of If ASBVd were to establish in New Zealand the Pathogens 1 34 avocado industry as at risk of yield losses, the in New Zealand. Bulletin of the New Zealand VA, Aluja M eds. The Avocado: Botany, disease on the Florida avocado industry. cost of control and restricted market access. It is Department of Scientific and Industrial Production and Uses. CABI, Wallingford. Pp. HortTechnology 20: 23–238. estimated that 50% tree losses due to any of these Research 67. 39 p. 380–422. Everett KR, Stevens PS, Cutting JGM 1999. diseases or their control would cost the New CABI 2014a. Phellinus noxius. Crop Protection Darvas J 1982. Etiology and control of some Postharvest fruit rots of avocado are reduced Zealand economy over $100 million, and 75% Compendium. CAB International. avocado fruit diseases. DSc (Agric) thesis, by benomyl applications during flowering. tree losses could reduce industry value by $150 Wallingford, UK. www.cabi.org/cpc. University of Pretoria, Pretoria, South Africa. Proceedings / New Zealand Plant Protection million. Such impacts would decimate the New CABI 2014b. Avocado sunblotch viroid. CAB 136 p. conference 52: 153–156. Zealand avocado industry. International. Wallingford, UK. www.cabi. Darvas JM, Kotze JM 1987. Avocado fruit Everett KR, Rees-George J, Parkes SL, Johnston org/cpc diseases and their control in South Africa. PR 2003. Predicting avocado fruit rots REFERENCES CABI 2014c. Raaelea lauricola. Crop Protection Yearbook, South African Avocado Growers’ by quantifying inoculum potential in the Aitken AG, Warrington IJ 2017. FreshFacts. Compendium. CAB International. Association 10: 117–119. orchard before harvest. Proceedings V New Zealand Horticulture. Plant & Food Wallingford, UK. www.cabi.org/cpc. Desjardins PR, Drake RJ, Atkins EL, Bergh World Avocado Congress (Actas V Congreso Research, Auckland, New Zealand. 42 p. CABI 2014d. Pseudocercospora purpurea (spot BO 1979. Pollen transmission of avocado Mundial del Aguacate): 601–606. www.freshfacts.co.nz. blotch). Crop Protection Compendium. CAB sunblotch virus experimentally demonstrated. Everett KR, Rees-George J, Pushparajah IPS, Allan Herbarium 2000. Nga Tipu o Aotearoa - International, Wallingford, UK. www.cabi. California Agriculture 33: 14–15. Manning MA, Fullerton RA 2011. Molecular New Zealand Plant Names Database. http:// org/cpc. Desjardins PR, Drake RJ, Sasaki PJ, Atkins EL, identification of Sphaceloma perseae (Avocado nzflora.landcareresearch.co.nz/ (accessed 7 Chupp C 1954. A monograph of the fungus Bergh BO 1984. Pollen transmission of Scab) and its absence in New Zealand. Journal February 2018). genus Cercospora. published by the author, avocado sunblotch viroid and the fate of the of Phytopathology 159: 106–113. Ann PJ, Chang TT, Ko WH 2002. Phellinus noxius Ithaca, New York. pollen recipient tree. Phytopathology 74: 845. Fletcher WA 1976. Avocado growing in New brown root rot of fruit and ornamental trees Crous PW, Braun U 2003. Mycosphaerella Desjardins PR, Saski PJ, Drake RJ 1987. Chemical Zealand. Orchardist of New Zealand 49: 220- in Taiwan. Plant Disease 86: 820–826. and its anamorphs. 1. Names published in inactivation of avocado sunblotch viroid on 228. Ann PJ, Lee HL, Huang TC 1999. Brown root rot Cercospora and Passalora: Mycosphaerella and pruning and propagation tools. California Formby JP 2014. Potential range of ambrosia of 10 species of fruit trees caused by Phellinus its anamorphs. CBS Biodiversity Series No. Avocado Society Yearbook 71: 259–262. beetle based on temperature range. http:// noxius in Taiwan. Plant Disease 83: 746–750. 1. Centraalbureau voor Schimmelcultures, Dodge C, Coolidge J, Cooperband M, Cosse A, www.dontmovefirewood.org/potential- Anonymous 2015. Costa Rico bans Mexican, Utrecht, The Netherlands. 571 p. Carrillo D, Stouthamer R 2017. Quercivorol range-ambrosia-beetle-based-temperature- Guatamalen avocados. The Packer. July 27. da Graca JV, van Vuuren SP 1980. Transmission as a lure for the polyphagous and Kuroshio range.html (accessed 10 February 2018). https://www.thepacker.com/article/costa- of avocado sunblotch disease to cinnamon. shot hole borers, Euwallacea spp. nr. Fraedrich SW, Harrington TC, Rabaglia RJ, rica-bans-mexican-guatemalan-avocados Plant Disease 64: 475. fornicatus (Coleoptera: Scolytinae), vectors of Ulyshen MD, Mayfield AE, III, Hanula JL, Anonymous 2018. AvoGreen Manual. Version da Graca JV, van Vuuren SP 1981a. Host range Fusarium dieback. Peerj 5. Eickwort JM, Miller DR 2008. A fungal 6.3. February 2018. www.nzavocado.co.nz. 33 studies on avocado sunblotch. South African EPPO 2016. Avocado sunblotch viroid symbiont of the redbay ambrosia beetle causes p. Avocado Growers’ Association Yearbook 4: (ASBVDO). https://gd.eppo.int/taxon/ a lethal wilt in redbay and other Lauraceae in Avila-Quezada GD, Teliz-Ortiz D, Mora-Aguilera 80. ASBVD0/distribution (accessed 17 April the southeastern United States. Plant Disease G, Vaquera-Huerta H, Tijerina-Chavez L da Graca JV, van Vuuren SP 1981b. Use of high 2018). 92: 215–224. 2003. Spatial and temporal dynamic of scab temperature to increase the rate of avocado Eskalen A, Gonzalez A, Wang DH, Twizeyimana Fraedrich SW, Harrington TC, Bates CA, Johnson (Sphaceloma perseae Jenk.) on avocado sunblotch symptom development in indicator M, Mayorquin JS, Lynch SC 2012. First report J, Reid LS, Best GS, Leininger TD, Hawkins (Persea americana Mill.). Revista Mexicana seedlings. Plant Disease 65: 46-47. of a Fusarium sp. and its vector Tea Shot TS 2011. Susceptibility to laurel wilt and de Fitopatologia 21: 152–160. da Graca JV, Mason TE, Antel HJ 1983. Effect Hole Borer (Euwallacea fornicatus) causing disease incidence in two rare plant species, Bates CA, Fraedrich SW, Harrington TC, of avocado sunblotch disease on fruit yield. Fusarium dieback on avocado in California. pondberry and pondspice. Plant Disease 95: Cameron RS, Menard RD, Best GS 2013. South African Avocado Growers’ Association Plant Disease 96: 1070. 1056–1062. First report of laurel wilt, caused by Raaelea Yearbook 6: 86–87. Eskalen A, Stouthamer R, Lynch SC, Rugman- Freeman S, Protasov A, Sharon M, Mohotti lauricola, on sassafras (Sassafras albidum) in Dann E, Smith L, Pegg K, Grose M, Pegg G Jones PF, Twizeyimana M, Gonzalez A, K, Eliyahu M, Okon-Levy N, Maymon M, Alabama. Plant Disease 97: 688. 2009. Report on Phellinus noxius, the cause Thibault T 2013. Host range of fusarium Mendel Z 2012a. Obligate feed requirement Boesewinkel HJ 1982. A list of 142 new plant of brown rot, in Australian avocados. Talking dieback and its ambrosia beetle (Coleoptera: of Fusarium sp. nov., an avocado wilting disease recordings from New Zealand and Avocados 20: 28–34. Scolytinae) vector in Southern California. agent, by the ambrosia beetle Euwallacea aff. short notes on three diseases. Australasian Dann EK, Ploetz RC, Coates LM, Pegg KG 2013. Plant Disease 97: 938–951. fornicata. Symbiosis 58: 245–251. Plant Pathology 11: 40–43. Foliar, fruit and soilborne diseases. In: Whiley Evans EA, Crane J, Hodges A, Osborne JL 2010. Freeman S, Protasov A, Wysoki M, Yehuda B, Brien RM 1939. A list of plant disease recorded AW, Schaffer B, Wolstenholme BN, Albert Potential economic impact of laurel wilt Noi M, Rabaglia R, O’Donnell K, Sharon Pathogens 1 35 avocado industry as at risk of yield losses, the in New Zealand. Bulletin of the New Zealand VA, Aluja M eds. The Avocado: Botany, disease on the Florida avocado industry. cost of control and restricted market access. It is Department of Scientific and Industrial Production and Uses. CABI, Wallingford. Pp. HortTechnology 20: 23–238. estimated that 50% tree losses due to any of these Research 67. 39 p. 380–422. Everett KR, Stevens PS, Cutting JGM 1999. diseases or their control would cost the New CABI 2014a. Phellinus noxius. Crop Protection Darvas J 1982. Etiology and control of some Postharvest fruit rots of avocado are reduced Zealand economy over $100 million, and 75% Compendium. CAB International. avocado fruit diseases. DSc (Agric) thesis, by benomyl applications during flowering. tree losses could reduce industry value by $150 Wallingford, UK. www.cabi.org/cpc. University of Pretoria, Pretoria, South Africa. Proceedings / New Zealand Plant Protection million. Such impacts would decimate the New CABI 2014b. Avocado sunblotch viroid. CAB 136 p. conference 52: 153–156. Zealand avocado industry. International. Wallingford, UK. www.cabi. Darvas JM, Kotze JM 1987. Avocado fruit Everett KR, Rees-George J, Parkes SL, Johnston org/cpc diseases and their control in South Africa. PR 2003. Predicting avocado fruit rots REFERENCES CABI 2014c. Raaelea lauricola. Crop Protection Yearbook, South African Avocado Growers’ by quantifying inoculum potential in the Aitken AG, Warrington IJ 2017. FreshFacts. Compendium. CAB International. Association 10: 117–119. orchard before harvest. Proceedings V New Zealand Horticulture. Plant & Food Wallingford, UK. www.cabi.org/cpc. Desjardins PR, Drake RJ, Atkins EL, Bergh World Avocado Congress (Actas V Congreso Research, Auckland, New Zealand. 42 p. CABI 2014d. Pseudocercospora purpurea (spot BO 1979. Pollen transmission of avocado Mundial del Aguacate): 601–606. www.freshfacts.co.nz. blotch). Crop Protection Compendium. CAB sunblotch virus experimentally demonstrated. Everett KR, Rees-George J, Pushparajah IPS, Allan Herbarium 2000. Nga Tipu o Aotearoa - International, Wallingford, UK. www.cabi. California Agriculture 33: 14–15. Manning MA, Fullerton RA 2011. Molecular New Zealand Plant Names Database. http:// org/cpc. Desjardins PR, Drake RJ, Sasaki PJ, Atkins EL, identification of Sphaceloma perseae (Avocado nzflora.landcareresearch.co.nz/ (accessed 7 Chupp C 1954. A monograph of the fungus Bergh BO 1984. Pollen transmission of Scab) and its absence in New Zealand. Journal February 2018). genus Cercospora. published by the author, avocado sunblotch viroid and the fate of the of Phytopathology 159: 106–113. Ann PJ, Chang TT, Ko WH 2002. Phellinus noxius Ithaca, New York. pollen recipient tree. Phytopathology 74: 845. Fletcher WA 1976. Avocado growing in New brown root rot of fruit and ornamental trees Crous PW, Braun U 2003. Mycosphaerella Desjardins PR, Saski PJ, Drake RJ 1987. Chemical Zealand. Orchardist of New Zealand 49: 220- in Taiwan. Plant Disease 86: 820–826. and its anamorphs. 1. Names published in inactivation of avocado sunblotch viroid on 228. Ann PJ, Lee HL, Huang TC 1999. Brown root rot Cercospora and Passalora: Mycosphaerella and pruning and propagation tools. California Formby JP 2014. Potential range of ambrosia of 10 species of fruit trees caused by Phellinus its anamorphs. CBS Biodiversity Series No. Avocado Society Yearbook 71: 259–262. beetle based on temperature range. http:// noxius in Taiwan. Plant Disease 83: 746–750. 1. Centraalbureau voor Schimmelcultures, Dodge C, Coolidge J, Cooperband M, Cosse A, www.dontmovefirewood.org/potential- Anonymous 2015. Costa Rico bans Mexican, Utrecht, The Netherlands. 571 p. Carrillo D, Stouthamer R 2017. Quercivorol range-ambrosia-beetle-based-temperature- Guatamalen avocados. The Packer. July 27. da Graca JV, van Vuuren SP 1980. Transmission as a lure for the polyphagous and Kuroshio range.html (accessed 10 February 2018). https://www.thepacker.com/article/costa- of avocado sunblotch disease to cinnamon. shot hole borers, Euwallacea spp. nr. Fraedrich SW, Harrington TC, Rabaglia RJ, rica-bans-mexican-guatemalan-avocados Plant Disease 64: 475. fornicatus (Coleoptera: Scolytinae), vectors of Ulyshen MD, Mayfield AE, III, Hanula JL, Anonymous 2018. AvoGreen Manual. Version da Graca JV, van Vuuren SP 1981a. Host range Fusarium dieback. Peerj 5. Eickwort JM, Miller DR 2008. A fungal 6.3. February 2018. www.nzavocado.co.nz. 33 studies on avocado sunblotch. South African EPPO 2016. Avocado sunblotch viroid symbiont of the redbay ambrosia beetle causes p. Avocado Growers’ Association Yearbook 4: (ASBVDO). https://gd.eppo.int/taxon/ a lethal wilt in redbay and other Lauraceae in Avila-Quezada GD, Teliz-Ortiz D, Mora-Aguilera 80. ASBVD0/distribution (accessed 17 April the southeastern United States. Plant Disease G, Vaquera-Huerta H, Tijerina-Chavez L da Graca JV, van Vuuren SP 1981b. Use of high 2018). 92: 215–224. 2003. Spatial and temporal dynamic of scab temperature to increase the rate of avocado Eskalen A, Gonzalez A, Wang DH, Twizeyimana Fraedrich SW, Harrington TC, Bates CA, Johnson (Sphaceloma perseae Jenk.) on avocado sunblotch symptom development in indicator M, Mayorquin JS, Lynch SC 2012. First report J, Reid LS, Best GS, Leininger TD, Hawkins (Persea americana Mill.). Revista Mexicana seedlings. Plant Disease 65: 46-47. of a Fusarium sp. and its vector Tea Shot TS 2011. Susceptibility to laurel wilt and de Fitopatologia 21: 152–160. da Graca JV, Mason TE, Antel HJ 1983. Effect Hole Borer (Euwallacea fornicatus) causing disease incidence in two rare plant species, Bates CA, Fraedrich SW, Harrington TC, of avocado sunblotch disease on fruit yield. Fusarium dieback on avocado in California. pondberry and pondspice. Plant Disease 95: Cameron RS, Menard RD, Best GS 2013. South African Avocado Growers’ Association Plant Disease 96: 1070. 1056–1062. First report of laurel wilt, caused by Raaelea Yearbook 6: 86–87. Eskalen A, Stouthamer R, Lynch SC, Rugman- Freeman S, Protasov A, Sharon M, Mohotti lauricola, on sassafras (Sassafras albidum) in Dann E, Smith L, Pegg K, Grose M, Pegg G Jones PF, Twizeyimana M, Gonzalez A, K, Eliyahu M, Okon-Levy N, Maymon M, Alabama. Plant Disease 97: 688. 2009. Report on Phellinus noxius, the cause Thibault T 2013. Host range of fusarium Mendel Z 2012a. Obligate feed requirement Boesewinkel HJ 1982. A list of 142 new plant of brown rot, in Australian avocados. Talking dieback and its ambrosia beetle (Coleoptera: of Fusarium sp. nov., an avocado wilting disease recordings from New Zealand and Avocados 20: 28–34. Scolytinae) vector in Southern California. agent, by the ambrosia beetle Euwallacea aff. short notes on three diseases. Australasian Dann EK, Ploetz RC, Coates LM, Pegg KG 2013. 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Susceptibility of species complex. Agricultural Forest Mail Centre, Christchurch 8140, New Zealand Persea spp. and other Lauraceae to attack by Entomology 19: 366-375. *Corresponding author: [email protected] redbay ambrosia beetle, Xyleborus glabratus Vidales F 1996. La rona Sphaceloma persea del (Coleoptera: Curculionidae: Scolytinae). aguacate Persea americana en Michoacan. Abstract The Tospovirus Iris yellow spot virus (IYSV), transmitted by thrips (predominantly Florida Entomologist 95: 783–787. INIFAP, Campo Experimental Urapon, CIR rips tabaci), was first recorded in New Zealand in 2007. In March 2015, symptoms of the Perez MRV, Ortiz DT, Almaraz RD, Martinez Pacifico Centro. Michoocan, Mexico. Folleto virus were relatively widespread in an organically managed onion crop in Canterbury. Onion JOL, Angel DN 2017. Avocado sunblotch Technico 4: 16. plants were sampled for the presence of T. tabaci adults and larvae and for IYSV symptoms viroid: Pest risk and potential impact in Vidales F, Alcantar R, Anguiano C 1999. Modelos on an organically managed farm in Canterbury in 2014–2015, 2015–16 and 2016–17, and Mexico. Crop Protection 99: 118-127. de prediccion de rona (Sphaceloma persea on a similar farm in Hawke’s Bay in 2014–2015 and 2015–16. An immunoassay was used to Pernezny K, Marlatt R 2007. Diseases of avocado Jenkins), del aguacate (Persea americana confirm the presence of IYSV in some symptomatic plants. In Canterbury, IYSV symptoms in Florida. Bulletin Florida Cooperative Mill. cv. Hass) en Michoacan. Informe de were less apparent in 2015–16 and no symptoms were observed in 2016–17. No IYSV Extension Service PP21: 3. investigacion en Aguacate. INIFAP, Campo symptoms were observed in the Hawke’s Bay onion crop, despite relatively high T. tabaci Peterson R, Grice K 1992. Cercospora spot Experimental Uruapan, CIR Pacifico Centro, numbers. The virus symptoms declined from when they were first observed in March 2015 of avocado. Proceedings of the Australian Michoacan, Mexico. 14 p. to undetectable levels in 2016–17 in Canterbury, which may be attributed to crop location, Avocado Growers’ Federation Conference. Wallace JM, Drake RJ 1962. A high rate of seed fewer thrips and the absence of a disease reservoir in volunteer Allium cepa plants or other Ploetz RC, Perez-Martinez JM, Smith JA, Hughes transmission of avocado sunblotch virus hosts. M, Dreaden TJ, Inch SA, Fu Y 2012. Responses from symptomless trees and the origin of of avocado to laurel wilt, caused by Raaelea such trees. Phytopathology 52: 237. Keywords Allium, onion thrips, rips tabaci, Tospovirus, Bunyaviridae, IYSV, viruliferous lauricola. Plant Pathology 61: 801–808. White J 2001. The Avocado Industry in New Ploetz RC, Konkol J 2013. First report of gulf Zealand. California Avocado Society licaria, Licaria trianda, as a suscept of laurel Yearbook 85: 77–91. wilt. Plant Disease 97: 1248–1249. Whiteside JO 1975. Biological characteristics INTRODUCTION tends to be localised, whereas other tosposviruses Pugh K, Thomson V 2009. Protecting our of Elsinoe fawcettii pertaining to the Onions (Allium cepa L.) are a widely used cause systemic infection (Smith et al. 2006). avocados. Biosecurity 93: 16–17. epidemiology of sour orange scab. vegetable around the globe. Iris yellow spot Disease symptoms are characterised by Rabaglia RJ, Dole SA, Cognat AI 2006. Review Phytopathology 65: 1170–1177. virus (IYSV) (Tospovirus: Bunyaviridae) is diamond- or spindle-shaped lesions on the leaf of American Xyleborina (Coleoptera: Zentmeyer G 1965. Avocado culture and avocado found throughout most onion-growing regions composed of chlorotic or necrotic tissue with, Curculionidae : Scolytinae) occurring North diseases in Australia and the South Pacific. of the world and is considered one of the most or without, a distinctive green centre (Gent et al. of Mexico, with an illustrated key. Annals of Californian Avocado Yearbook 49: 19–26. damaging viruses to attack onion crops (Gent et 2004). The resultant decline in photosynthesis the Entomological Society of America 99: al. 2006; Bag et al. 2015). The virus is transmitted leads to reduced bulb size (Gent et al. 2004). The 1034–1056. in a persistent, propagative manner by thrips main method for managing IYSV is through Saucedo-Carabez JR, Teliz-Ortiz D, Ochoa- vectors, similar to other tospoviruses (Gent reducing populations of thrips vectors, generally Ascencio S, Ochoa-Martinez D, Vallejo-Perez et al. 2006), with onion thrips ( rips tabaci) with the application of insecticides. However, MR, Beltran-Pena H 2014. Effect of Avocado considered the main vector. However, recent growers of organically produced of onions in sunblotch viroid (ASBVd) on avocado yield research has shown the virus can be transmitted New Zealand are only allowed to use natural in Michoacan, Mexico. European Journal of less efficiently by Frankliniella fusca, a thrips pyrethrums with restrictions (AsureQuality Plant Pathology 138(4): 799-805. species not present in New Zealand (Srinivasan 2018). Smith JA, Mount L, Mayfield AE, III, Bates et al. 2012). Unlike other tospoviruses, IYSV has IYSV was first reported in New Zealand in CA, Lamborn WA, Fraedrich SW 2009. a relatively narrow host plant range (Gent et al. 2007 in samples of Allium species collected from First report of laurel wilt disease caused by 2006; Smith et al. 2011). Infection by IYSV also the North and South Islands (Ward et al. 2009).